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Four New Species of Provanna (Gastropoda: Provannidae) from Vents and a Seep Off Nansei-Shoto Area, Southwestern Japan

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Four New Species of Provanna (Gastropoda: Provannidae) from Vents and a Seep Off Nansei-Shoto Area, Southwestern Japan VENUS 74 (1–2): 1–17, 2016 New Species of Provanna from SW Japan ©Malacological Society of Japan1 Four New Species of Provanna (Gastropoda: Provannidae) from Vents and a Seep off Nansei-shoto Area, Southwestern Japan Takenori Sasaki1*, Tomomi Ogura2,3, Hiromi Kayama Watanabe3 and Katsunori Fujikura2,3 1The University Museum, The University and Tokyo, 7-3-1 Hongo, Bunkyo-ku, Tokyo 113-0033, Japan 2Graduate School of Marine Science and Technology, Tokyo University of Marine Science and Technology, 4-5-7 Konan, Minato-ku, Tokyo 108-8477, Japan 3Japan Agency for Marine-Earth Science and Technology, 2-15 Natsushima-cho, Yokosuka-shi, Kanagawa 237-0061, Japan Abstract: Members of the genus Provanna are abundant and widely distributed in deep-sea chemosynthetic environments. Around Japan provannids inhabit a wide range of depths and substrates. In this study, we report additional species of Provanna from vents and a seep in the Nansei-shoto area. Shell morphological and molecular phylogenetic analyses showed that there are four new species: (1) P. subglabra is characterized by an inated smooth shell and is most abundant in vent elds in the Okinawa Trough; (2) P. clathrata has a roughly sculptured shell and is distributed in vents in the southern Okinawa Trough; (3) P. lucida possesses a thin smooth shell with a deep suture and is limited to vents on the Minami-Ensei Knoll in the northern Okinawa Trough; and (4) P. kuroshimensis, which is distinguished by an olive-colored periostracum and is endemic to a seep site on the Kuroshima Knoll. In contrast to shell and molecular characters, radula morphology does not show clear differences among these species. The present study revealed a high species diversity of Provanna in a relatively limited area in southwestern Japan. The diversication of the genus might be correlated with complex topographic features in the Nansei-shoto area including the Okinawa Trough and Ryukyu Arc. Keywords: Provannidae, Provanna, new species, Nansei-shoto area, Okinawa Trough, Japan Introduction The genus Provanna is one of the most abundant and widely distributed taxa in deep-sea chemosynthetic communities, including hydrothermal vents, hydrocarbon seeps, sunken wood and vertebrate falls. They are considered to be deposit feeders and grazers on bacterial mats and detritus (Sasaki et al., 2010). Molecular phylogenetic analyses have indicated that the Recent lineages of Provanna could have radiated about 15–45 million years ago (Johnson et al., 2010), and actual fossil records of Provanna trace back to the Cenomanian age in the Late Cretaceous epoch (Kaim et al., 2008). Up to now the genus has been composed of 25 valid species (see discussion for details) including 18 extant (Warén & Bouchet, 1986, 1993, 2009; Okutani, 1990; Warén & Ponder, 1991; Okutani, 1990; Okutani et al., 1992; Okutani & Fujikura, 2002) and seven fossil species (Squires, 1995; Kaim et al., 2008, 2009; Saether et al., 2010; Amano & Jenkins, 2013; Amano & Little, 2014). Among them only three living species have been known from the northwestern Pacic: (1) Provanna abyssalis has been collected from a methane seep site at a depth of 5,379 m on the * Corresponding author: [email protected] DOI: http://doi.org/10.18941/venus.74.1-2_1 2 T. Sasaki et al. landward slope of the Japan Trench (Okutani & Fujikura, 2002); (2) P. shinkaiae was reported from another methane seep site at 5,343 m on the same landward slope (Okutani & Fujikura, 2002); (3) Provanna glabra inhabits a methane seep at depths around 1,100 m off Hatsushima Island, Sagami Bay (Okutani et al., 1992; Sasaki et al., 2007). A species of Provanna from the Okinawa Trough was previously identied as P. glabra, but it was later regarded as a separate species, based on differences in shell morphology (Sasaki et al., 2005, 2010). In addition, another similar species was collected from a seep on the Kuroshima Knoll which is the type locality of two species of Bathymodiolus (Okutani et al., 2004). Including these unnamed species, we describe four new species from Japan in this study. Material and Methods Study sites and sampling: Specimens of Provanna were collected from 10 sites around Japan between May 2002 and October 2011 during dives of the human-occupied vehicles (HOVs) Shinkai 2000 and Shinkai 6500 and the remotely operated vehicles (ROVs) Dolphin-3K, Hyper-Dolphin, Fig. 1. Map of the sampling locations. a, whole map; b, magnied map of the Nansei-shoto area. Circles, methane seep sites; triangles, hydrothermal vent sites. 1, Off Hatsushima Island site; 2, Minami-Ensei Knoll; 3, North Knoll of Iheya Ridge; 4, Iheya Ridge; 5, Izena Hole; 6, Irabu Knoll; 7, Hatoma Knoll; 8, Dai-yon Yonaguni Knoll; 9, Kuroshima Knoll. See Table 2 for geographic distribution of known Provanna species. New Species of Provanna from SW Japan 3 Table 1. List of sampling locations in this study. Number of sampling site corresponds to number in Fig. 1. No. Site Latitude Longitude Depth Habitat 1 Off Hatsushima Island, Sagami Bay 35°00′N 139°14′E 1,172 m Seep 2 Minami Ensei Knoll 28°24′N 127°38′E 701 m Vent 3 North Knoll of Iheya Ridge 27°48′N 126°54′E 982 m Vent 4 Iheya Ridge 27°33′N 126°58′E 1,399 m Vent 5-1 JADE site in Izena Hole 27°16′N 127°04′E 1,309 m Vent 5-2 HAKUREI site in Izena Hole 27°15′N 127°04′E 1,617 m Vent 6 Irabu Knoll 25°14′N 124°52′E 1,646 m Vent 7 Hatoma Knoll 24°52′N 123°51′E 1,473 m Vent 8 Dai-yon Yonaguni Knoll 24°51′N 122°42′E 1,387 m Vent 9 Kuroshima Knoll 24°08′N 124°12′E 644 m Seep and Kaiko 7000II of the Japan Agency for Marine-Earth Science and Technology (Fig. 1; Table 1). Live-collected specimens were xed and preserved in 99.5% ethanol or frozen. Morphological analyses: Species identication of Provanna has been based on shell and radular morphology (Warén & Ponder, 1991), and we also utilized these characters for morphological observations. We also performed morphometric analysis of the shell characters. Shell: Photographs of shells were taken using a digital camera system (ACT2-U) attached to a compound microscope system (MZ-3; Leica Microsystems). Seven shell morphology parameters, namely shell width (SW), height of body whorl (HBW), height of aperture (HA), width of aperture (WA), width of suture (WS), width of penultimate whorl (WP), and apical angle of shell (AS), were measured for all available spec imens in photos using Image J software (Abràmoff et al., 2004), which was installed in the ACT2-U system. Depth of suture (DSt) was calculated using the following equation: DSt = (WP – WS)/2. To compare the proportion of shells among different size samples, HBW and WA were divided by WA and SW, respectively, to minimize the effect of size variation. Additionally, measurements of the thickness of the peristome (TP), shape of aperture, and sculpture were obtained for species comparison. TP, DSt, and aperture were transformed into arbitrarily scored data based on whether it was thick or thin, sculptured or not sculptured, or pyriform or not pyriform in shape. The obtained morphometric data, HBW/SW, HA/WA, DSt, AS, and TP, were standardized to Euclidean distances. The standardized variables were transformed into a resemblance matrix, which was calculated using the Euclidean distances and used to perform cluster analysis using the SIMPROF test, with the level of signicance set as α = 0.05. These statistical analyses were performed using PRIMER-E ver. 6 (Clarke & Gorley, 2006). Radula: Radulae were extracted from ethanol-xed specimens, cleaned in a diluted solution of commercial bleach, and mount ed on double-sided carbon tape (8 mm × 20 m; Nissin EM Corporation, Tokyo, Japan) under a compound microscope. The tape-mounted radulae were examined using a scanning electron microscope (TM3000; HITACHI Ltd., Tokyo, Japan). DNA extraction and amplication: Genomic DNA was extracted from the foot muscle, using the DNeasy Tissue Extraction Kit (QIAGEN). Each 1 μL genomic DNA was puried using GeneReleaser (BioVentures Inc., Marf reesboro, USA), following the manufacturer’s protocol. Two fragments of the mitochondrial cytochrome c oxidase subunit I (COI) were amplied by polymerase chain reaction (PCR) using the primer set LCO1490 and HCO2198 (Folmer et al., 1994), and newly designed primers, Pg501L (5′-TATACGATGACGGGGAATGC-3′) and Pg1253R (5′-TGTTGAGGAAAGAAAGTAATATTAA-3′) and combined into a single 1,044-bp sequence. In additi on, a 441-bp sequence of the 16S ribosomal RNA (16SrRNA) and a 434-bp sequence of the 4 T. Sasaki et al. 28S ribosomal RNA-D6 (28SrRNA-domain 6) were amplied using two primer sets, 16Sar and 16Sbr (Palumbi, 1996), and 28SD6F (McArthur & Koop, 1999) and 28SD6R (Colgan et al., 2003), respectively. PCR was conducted in a 20-μL solution that included 3 μL of puried template DNA, 11.3 μL of deionized sterilized water, 2 μL of 10 × PCR buffer, 1.5 μL of 2.5 mM dNTP, 1 μL of each primer and 0.2 μL of 5 U/μL Ex Taq DNA polymerase (TaKaRa Bio Inc., Ohtsu, Japan). PCR amplication of COI fragments was carried out using an initial denaturation step of 94°C (120 s), followed by 30 cycles consisting of a denaturation step at 94°C (30 s), an annealing step at 45°C (30 s), and an extension step at 72°C (30 s), and nally an extension at 72°C (40 s). DNA sequencing: The PCR products were puried using ExoSAP-IT® (USB®, Affymax , Santa Clara, USA). The puried PCR products were subjected to a cycle sequencing reaction using the BigDye® Terminator Cycle Sequencing Kit Version 3.1 (Applied Biosystems®, Life Technologies Corporation, Carlsbad, USA).
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